,' ,' u. Mar& Biology 116, 439-450 (1993) Marine View metadata, citation and similar papers at core.ac.uk brought to you by CORE "2II-wI.,c. Biology-- 0 Springer-Verlagprovided by 1993 Horizon / Pleins textes

Reproductive biology of the holothurians from the major communities of the New Caledonian Lagoon C. Conand Laboratoire d'océanographie Biologique, URA C.N.R.S. D1513, Université de Bretagne Occidentale, 29275 Brest Cedex, France

Received: 5 January 1993 / Accepted: 18 February 1993

Abstract. The reproductive biology of nine of as- both benthic ecology to understand their structure and pidochirote holothurians from the major communities of functioning, and on the biology of the various halieutic the New Caledonian lagoon has been analysed. The data resources. The holothurian fauna is particularly rich, ca. were obtained from monthly sampling from 1978 to 1982 60 species, amongst which aspidochirotes are dominant of their populations on reef slopes and passes for with ca. 50 species (Guille et al. 1986, Conand 1989a). nobilis, H. fuscogilva, H. fuscopunctata and The main affinities and associations of these aspidochi- ananas, in the inner lagoon for varie- rotes have been detailed in an ecological study conducted gatus, H. scabra and H. scabra versicolor and on reef flats on the scale of the wholeiagoon (Conand and Chardy for? mauritiana, A. echinites and H. atra. The 1985). The purpose of the present paper is to describe the morphology and anatomy of the gonads and their annual reproductive biology of nine common species character- cycle are described. The reproductive cycles, composed of istic of the major communities. This set of data concern- the five phases of gonad growth, maturing, spawning, ing species at the same taxonomic level allows a synthesis post-spawning and resting, were determined from the of their reproductive biology and makes it possible to changes in the sexual stages, the gonad indices and the relate their adaptative strategies to their distribution and percentage of indeterminate sex. Three main reproduc- abundance. tive patterns are recognized, annual cycles with spawning occurring during the warm season or during the cool season and a semiannual cycle. Other population Materials and methods parameters, such as the size of the mature oocytes, the m5an size of the individuals at first sexual maturity, and The different species were collected from the southwest lagoon (Fig. 1) at sites where the populations are dense. These species are absc&e and relative fecundities were calculated and re- characteristic of the main holothurian communities defined by Co- lated to the mean size of the species, the and nand and Chardy (1985). the ecology. The reproductive strategies of the species Holothuria nobilis, H. fuscogilva. H.fuscopunctata and Theleno- show a gradient that is probably related to the stability of ta ananas are characteristic of the reef slopes and passes (infralit- the biotopes, with smaller species living in the more in- toral reef community). In general, their populations are composed stable outer reef flats and larger species in deeper lagoon of large individuals with rather low densities (Conand 1989a). Holothuria scabra versicolor (described in Conand 1986) and floors. Stichopus variegatus are characteristic of the inner lagoon (terrige- nous infralittoral community), while H. scabra is more coastal. Compared with the first group, the populations are composed of medium-sized individuals with intermediate densities. Introduction Actinopyga niiliaris and Holothuria atra are a very common and characteristic species of the inner reef flats (terrigenous mediolit- toral community). Compared with the second group, the popula- Holothurians are conspicuous commonly tions are composed of smaller individuals with high densities. found in the various coral-reef and lagoon benthic com- Actinopyga inauritiana and A. echinites are characteristic of the munities, but little is known about their biology and their outer reef flats (mediolittoral reef community). The populations of ecological role (Bakus 1973, Birkeland 1989). The New these two species are composed of smaller individuals with variable Caledonian lagoon and reefs are very diversified and densities that can be very high. complex. A number of studies have been conducted, on The sampling methods and laboratory measurements used were those of Conand (1981, 1986, 1989a) and are described briefly below. Microscopic examination of fresh and formalin preserved Present address: Université de la Réunion, Laboratoire de Biologie gonads was used to establish the sex and maturity stage and to Marine, 15 Avenue René Cassin, 97489 Saint-Denis, Cédex, France measure the oocyte diameters. A maturity scale in five stages, estab- $ - WOU\ 1994 O. R.S.T.O. M. Fonds Documentaire *' 440 C. Conand: Reproduction of New Caledonian holothurians

Fig. 1. Sampling sites of holothurians in the lagoon of New Caledonian

lished for Holothuria nobilis, H. fuscogilva, (Co- with developing or developed gonads against classes of drained nand 1981), Actinopyga echinires (Conand 1982) and Stichopus var- weight (Conand 1981). In order to indicate the relative position of iegatus (Conand 1993), was used. The stage of maturity was deter- the first maturity in the entire life-cycle, the ratio of LT,, and WD,, mined by criteria including: form, color, consistency and weight of to the maximum values of LT and WD (LTu and WD,) were the gonads, the length and diameter of the fecund tubules, and the calculated. size and microscopic characteristics of the oocytes. Stages I and II Fecundity was estimated from mature ovaries in stage IV. It was (undetermined) are gonads whose sex could not be established. assumed that oocytes in the most advanced mode, as indicated by Stage I corresponds to immature gonads and stage II to resting the size frequency distribution, are spawned during the reproductive gonads, stage III corresponds to developing gonads, stage IV to season and that their number corresponds to the absolute fecundity. maturing and spawning gonads, and stage V to post-spawning go- An ovary sample of known weight (g) was fixed in Gilson's fluid nads. (Bagenal 1973), the oocytes volumetrically subsampled and the The reproductive cycles were established through the combined number of oocytes (n) in the most advanced mode counted. The use of three criteria: the monthly percentages of the maturity stages absolute fecundity (FA) was calculated as FA=n (GW/g). The rel- for each sex, the monthly gonad index (GI), the ratio of the wet ative fecundities (FRO: fecundity related to eviscerated weight; gonad weight (GW) to the drained body weight (WD) and the FRG: fecundity related to ovary weight) were calculated as monthly percentage of individuals that could not be sexed. Five FRO = FA/GW =n/g, per gram ovary, and FRG = FA/WG, per phases were distinguished. A growing phase with an increase of body wall (eviscerated) gram weight. gonad index and preponderance of stage III gonads, a maturing Bimonthly mean seawater temperatures were calculated from phase with the highest gonad index and increase in percent of daily measurements at the Noumea coastal station (Fig. 1). stage IV gonads, a spawning phase with a sharp decrease in the gonad index and increase in percent of stage V gonads, a post- spawning phase with a continuous decrease in the gonad index and Results a resting phase with the lowest gonad index and a maximum of stages I and II. Sex ratio, gonad anatomy, maturity stages First sexual maturity for a population was defined as the size (LTs0). or weight (WD,,), at which the gonads of 50% of the individuals were undergoing gametogenesis during the reproductive All the species studied are dioecious. The sex-ratios (per- season. It was determined by plotting the percentage of individuals centage of males) are given in Table l. The Chi-square C‘. Conand: Kcproduction 01‘ Ncw Calcdonian holorhurians 44 1

Fig. 2. Anatomy of Stichopodid gonads. Branched tubules with saccules in Thelenota u~iui~as:(A) stage I, II; (B) ovary, stage IV. t: tubule; s: saccule. Unbranched tubules with saccules in Stichopus variegatus: (C) ovary, stage IV; (D) testis, stage V

Table 1. Sex-ratio of holothurians. M: males; F: The gonads show very similar morphologies in the seven females species of Holothuridae studied. They are more variable amongst (Conand 1993). In one group. Habitat the tufts are composed of elongated tubules similar to Species those in the Holothuridae. In a second group, short Slopes and passes branches of saccules develop from the tubules which are Holorliroiu tiohilk 239 242 50 branched in Tiieletiotu unatias and Sticliopiis chlorotiorus Holo I li uriu Jiiscog il I‘(/ 51 50 53 but not in S. scwieggatw, as shown in Fig. 2. Spicules are Holothuriu fiiscopimcrcrta 119 104 53 very abundant in the gonad wall of these species. Thelerzata aizaiins 127 116 52 The main features of the mature gonads (stage IV) are Outer reef ilats presented i6 Table 2. Sexual dimorphism is evident at this Acti/lOp~gLI/~it/l//.iri[l/Itr 134 124 52 stage. The fecund ovarian tubules are shorter and wider. Actitiopj.gu echi/iircs ‘43 227 52 the ovaries are heavier than the testes. and the gonad Inner lagoon and rcef Ilats index mean values are higher for females than males. Holodiirriu utr0 61 56 54 Interspecific differences are also conspicuous at this Holorhrrriu sctrhrir 160 132 55 Holorh~rritr.swhrtr ~rsi~lor 149 113 57 stage, as shown in Fig. 3 where the mean ovary weight St id1 opus ~“k,g(riris 100 114 47 and female gonad index at stage IV are related to the mean body wall weight of each species at the sampling site (data from Conand 1989 a). Amongst Holothuridae. the large species such as Holothu~icr~u.scoputic.fntaor H. test indicated that the sex-ratios are not significantly dif- tzobifis generally have the largest gonads and small species ferent from 1, except for Holotliuria scabru versicolor have smallcst ones (Table 3). The maximal values show (x2=4.94. p =0.05, ti = 767). the same relation with size. such as for example the The gonads consist of one tuft of tubules in the family “record gonads” weighing 370 g in an ovary of H.Jii.sco- Holothuridae and two tufts in the family Stichopodidae. pwicrata and H. riobilis. The same figure was obtained for - A O -I- 100- n Srichopodldoa *io I i -o AO $ 5 W -0 > O O 0 a- Ha -4 >< z Am.. O O O Q Hsv nn Hfp w2 . 4 60- 3 Fig. 3. Mean ovary weight and female . u- gonad index at stage IV, in relation to m the mean body wall weight of the O Am species. Hn: Holothuria nobilis; Hfg: AO0 O& e H:g H. fïscogilva; Hfp: N.fuscopunctata; m- Hs: H. scabra; HSV:H. scabra versicolor; m Ae: Actinopyga eclrinites; Am: A. mauri- tiana; SV: StichOpus variegatus; Ta: T ananas. o: member of O Stichopodidae family o,, I I 1 1

Table 2. Characteristics of mature gonads of New Caledonia holothurians. M: males; F: females; n: number of specimens; GW: mean wet gonad weight (standard deviation); oocyte 0:modaldiameter of the most advanced mode after formalin fixation; mean gonad index: (GW x lOO)/WD (standard deviation); WD: drained weight (g)

Family Sex n GW (g) Tubules Gonad index Oocyte Species mean (SD) mean (SD) (pm) Length ("1 TB (-1 Holo thuridae Holothuria nobilis M 83 50.6 (36.8) i 23 1.1 3.5 (2.1) F 109 77.7 (63.1) 103 2.0 5.3 (3.0) 150 M 27 13.8 (14.0) 88 0.9 0.8 (0.8) F 21 36.0 (30.6) 79 1.6 2.2 (1.7) 170 Holothuria fuscopunctata M 52 45.2 (29.6) 159 1.1 2.2 (1.1) F 54 78.5 (57.8) 118 1.9 4.0 (2.2) 210 Actinopyga mauritiana M 61 32.2 (22.8) 153 1.0 7.1 (4.2) F 64 32.9 (22.5) 124 1.5 7.2 (4.2) 170 A ctinopyga echìn ìtes M 96 20.9 (12.5) 115 0.8 6.9 (3.6) F 80 28.2 (16.6) 106 1.2 9.0 (4.7) 165 Holothuria scabra M 74 23.8 (12.6) 82 1.o 5.4 (2.4) F 65 31.2 (21.3) 80 1.3 7.2 (3.8) 190 Holothuria seabra versicolor M 72 45.9 (27.0) 137 1.3 4.0 (1.7) F 53 69.7 (43.6) 125 1.9 5.8 (2.8) 210 Holothuria atra M 26 5.5 (5.0) 67 1.6 3.3 (2.6) F 21 7.4 (6.4) 65 2.1 3.3 (1.4) 150

Stichopodidae Thelenota ananas M 42 26.1 (15.9) 165 1.1 (0.5) F 49 37.9 (27.7) 158 1.6 (1.0) 200 Stichopus variegatus M 20 34.1 (29.0) 278 2.8 (1.9) F 32 36.4 (22.4) 254 2.1 (1.5) 180 males, with smaller gonad weights and gonad indices. In consisted of large residual oocytes, degenerating oocytes Stichopodidae, the gonads are not as large as in and occasional empty follicules. Holothuridae of the same size. The modal diameter of the I oocytes of the last mode of the size frequency distribution (Table 2) is between 150 and 210 Dm. Tubule resomion Reproductive cycles and spawning behaviour in spawned individuals occurred' over several mdnths. The annual reproductive cycle for each species was Apart from small oocytes, the ovary of these individuals analysed from observations over two or more years, at . I

-"-- . . C. Conand: Reproduction of New Caledonian holothurians 443 one or more sites. As the timing and duration were simi- reproductive cycles and the hydrological seasons are lar over years and sites, the monthly data have been summarised in Fig. 4. Three main patterns are evident. pooled and a single annual cycle is presented. The three An annual cycle, with spawning during the warm season, sets of monthly observations, respectively, the percent- occurred in most species. An annual cycle, with spawning ages of stages III, IV, V in males and females, the percent- during the cool season, occurred in one species, age of individuals that could not be sexed and the mean Holotliuria nobilis. A semi-annual cycle, with the main gonad index are given for each species (Table 3). The spawning during the warm season, occurred in H. scabra and perhaps in H. atra. Some characteristics of broadcast spawning in the field are summarised in Table 4. The anterior half of the spawning individual was raised in a vertical position with the tentacular crown curved toward the substratum. The genital papilla posterior to the tentacles was extended. The individual weaved slowly, before and during shed- ding. The sperm formed a white string more easily distin- guished than the translucent eggs. This behaviour is illus- trated in Fig. 5 for Bolzadschia argus, Holothuria scabra versicolor and Sticlzoplus variegatus where a small sperm stream is coming out the genital papilla.

Size at first sexual maturity and fecundity

The percentage of individuals ripening during the repro- ductive season increases with size, from O to nearly 100%. The length at first maturity (LTs0),as well as the weights at first maturity, total wbkht (WT,,) and drained weight (WD50) are given fÒr the different species in Table 5. The values are higher for the large species inhabiting the reef slopes and passes. They exceed 50% of the maximum length and 30% .of the maximum drained weight in Holotliuria fuscogilva, Actinopyga mauritiana and H. atra. -past spawning aresting The fecundity values are given in Table 6. Absolute fecundity values are variable within and between species. Fig. 4. Reproductive cycles of New Caledonia holothurians in rela- tion to hydrological seasons. H.: Holothuria; A.: Actinopyga; T.: Within a species, e.g. in Holothuria fuscopunctata, the Thelenota; S.: StichOpus maximal fecundity is 45-fold greater than the minimal

Fig. 5. Spawning behavior in the field (photographs by ORSTOM divers). (A) argus; (B) Holothuria scabra versicolor, (C) StichOpus variegatus I 444 C. Conand: Reproduction of New Caledonian holothurians

Table 3. Reproductive cycle of New Caledonia holothurians. II: number; I: undetermined individuals (%); M: male; F: female; III, IV, V: maturity stages (%); GI: mean gonad index; s: standard deviation

Species Month

J F M A M Ju Ji A S O N D

Holot huria n: 35 36 52 41 39 31 63 42 12 55 46 44 nobilis I: 3 8 2 2 2 3 4 4 7 5 2 20 Sex: MF MF MF MF MF MF MF MF MF MF MF MF III: O0 13 11 25 25 20 8 40 O0 O0 O0 O0 o4 O0 o3 IV: O6 13 22 50 20 46 72 86 100 100 87 70 76 19 26 50 29 20 27 10 12 6 10 V: 100 94 73 67 25 45 33 20 90 O 13 30 24 81 74 50 71 80 69 90 88 94 87 GI: 0.71 2.15 1.38 2.63 3.89 5.68 5.17 1.40 1.90 1.90 . 1.54 I .63 S: 1 .o5 2.09 1.85 2.15 2.50 3.84 4.18 1.24 1.10 1.10 1.59 1.55

Hololhuria 11: 17 34 41 40 39 17 16 32 21 21 26 20 scabra I: 6 2 9 15 23 24 O 3 9 4 7 5 Sex: MF MF MF MF MF MF MF MF MF MF MF MF ru: O0 O0 O0 O0 O0 O0 O0 11 10 7 17 11 16 O0 rv: 60 83 63 50 8 41 11 42 18 14 O0 67 50 62 55 33 10 93 83 89 84 80 89 V: 40 17 37 50 92 59 89 58 82 86 100 100 33 50 38 45 56 80 O0 O0 20 11 GI: 5.33 3.01 2.75 2.73 2.27 0.95 3.55 4.42 2.30 6.66 7.58 7.69 S: 2.81 2.01 1.33 1.67 1.82 0.51 2.38 3.27 2.03 3.34 5.03 4.60

Holothuria il: - 33 32 34 35 16 - 16 17 31 28 30 scabra versicolor I: 3 O 9 9 O 6 6 O 3 O Sex: MF MF MF MF MF MF MF MF MF MF rn: O0 O0 O8 O0 O0 60 40 50 38 O0 O0 o7 rv 50 47 28 43 il 25 O6 30 O 10 20 50 50 100 100 100 100 88 62 V: 50 53 72 57 89 67 100 94 70 100 30 40 o 12 O0 O0 12 31 GI: 3.86 1.79 1.33 0.80 1.99 1.99 2.72 5.59 5.18 3.72 S: 3.14 1.01 1.24 0.75 0.78 1.28 1.64 2.62 2.51 1.90

Holothuria II: 18 - 6 17 - - 27 - 19 - 26 12 fuscogilva I: 11 O 35 15 11 8 O Sex: MF MF MF MF MF MF MF I III: O0 O0 o 25 50 46 ' 13 o 14 20 O0 IV O 27 O0 O0 10 o 87 78 79 80 89 O v 100 73 100 100 100 75 40 54 o 22 70 11 100 GI: 0.99 0.13 0.04 0.21 0.59 1.18 1.21 S: 1.72 0.10 0.03 0.24 0.51 1.22 1.69

Holothuria t1: - 33 28 33 24 - 18 - 17 18 32 26 fuscopunctata I: 3 11 O 4 50 29 11 3 4 Sex: MF MF MF MF MF MF M. F MF MF III: 12 7 O0 O0 o 11 20 25 20 o 57 56 25 12 11 o VI: 53 73 54 75 32 36 70 O0 O0 O0 75 88 89 100 V: 35 20 46 25 68 64 93 89 80 75 80 100 43 44 O0 O0 GI: 1.98 2.47 1.10 0.54 0.37 0.53 0.97 3.22 2.82 S: 1.79 2.1 1 0.60 0.45 0.29 0.40 0.73 2.39 1.43 Holothuria atra n: 31 24 27 24 24 - 22 15 21 28 37 34 r: 32 58 48 84 83 82 73 81 61 30 38 sex: MF MF MF MF MF MF MF MF MF MF MF III: O0 O0 O0 O0 O0 O0 O0 O0 71 33 42 14 9 40 VI: 33 22 71 67 56 20 O0 O0 O0 O0 O0 29 O 50 79 18 30 V: 66 78 29 33 44 80 100 100 100 100 100 100 100 100 100 120 O 60 87 73 30 GI: 1.12 2.23 0.78 0.39 0.64 0.99 0.99 0.40 2.25 2.66 2.50 S: 0.76 1.58 0.77 0.26 0.29 0.94 0.54 0.31 2.07 1.82 2.43

Acrinopyga 11: 42 33 26 99 - 53 - - 26 33 6 77 mauritiana I: 53 45 57 O 13 O 48 O 19 Sex: MF MF MF MF MF MF MF MF MF ri[: O0 O0 O0 O0 56 76 36 42 33 9 O0 o3 rv: 90 O0 O0 O0 O0 64 50 67 91 66 100 100 94 V: 91 100 100 100 100 100 100 100 44 24 O8 O0 33 o o3 GI: 1.37 0.71 0.36 0.19 0.21 0.33 4.16 1.53 8.56 S: 3.36 0.74 0.34 0.28 0.25 2.23 2.08 1.22 4.60 Actinopyga n: 61 70 36 66 39 25 19 38 17 16 59 50 echiiiires r: 3 13 11 42 33 60 21 18 6 O O 12 Sex: MF MF MF MF MF MF MF MF MF MF MF MF ru: O0 O0 O0 O0 O0 O0 75 82 84 53 50 100 92 100 3 14 O0 rv: 89 100 10 3 O6 O0 O0 O0 O0 O0 O0 O0 97 83 100 100 V: 11 o 90 97 100 94 100 100 100 100 100 100 25 18 16 47 50 o O0 o3 O0 GI: 6.56 2.93 1.61 1.1 1 0.54 0.32 0.36 0.67 1.06 1.77 8.19 9.48 S: 4.04 3.18 1.64 1.64 0.63 0.40 0.27 1.02 0.78 1.07 4.55 3.15 C. Conand: Reproduction of New Caledonian holothurians 445

Table 3 (continued)

Species Month

J F M A M Ju Ji A S O N D

TIJCICYJOMI IJ: 31 29 37 28 32 17 16 17 - 23 41 UlJO1JU.S I: 23 3 8 11 16 12 44 59 17 IsO 17 Sex:MF MF MF MF MF MF MF MF MF MF MF III: 17 25 5 O O O O O 8 7 O 14 O O 67 83 89 80 25 57 42 47 IV: 83 75 50 86 19 70 i5 67 8 14 12 14 O O O O O O 75 43 58 53 V: O O 45 14 81 30 85 33 84 79 88 72 100 100 33 17 1120 O0 O0 G: 1.39 0.79 0.58 1.03 0.26 0.41 0.12 0.07 0.1 1 0.90 0.95 s: 1.13 0.5 I 0.59 0.98 0.34 0.41 0.1 i 0.02 0.07 0.72 0.94

Sriciro/~tls 11: 17 28 27 34 36 15 - 16 IO 16 16 17 variegul~is I: o 25 11 24 39 13 25 30 O 6 O Sex:MF MF MF MF MF MF MF MF MF MF MF III: O 12 O 14 O O O 11 IO O O O O0 O50 5789 5044 O0 IV: O O 14 14 15 18 O O O O O O O O O O O O 50 56 100 100 V: 100 88 86 72 85 82 100 89 90 100 i00 100 100 100 100 50 43 11 O O O O GI: 2.31 1.41 1.15 0.51 0.35 0.30 0.25 0.22 0.49 1.38 3.33 s: 2.05 1.34 1.08 0.40 0.20 0.21 0.08 0.09 0.32 0.78 2.00

Table 4. Direct field observations of holothurians spawning in New Caledonia. HT: high tide; MT: medium tide; LT: low tide; NM: new moon: FQ: first quarter; FM: full moon; LQ: last quarter

Species Observation Source Locality Date/time/environment

Actitzopyga miliaris 3 ind. amongst 15 seen Conand 1989a Devarenne Reef 8 Mar 1983/16:00 hrs/HT; LQ Holothuria flavoinaculata 2 ind. amongst 2 ._ Actinopyga miliaris Several ind. Conand 1989a Bailly Islet 3 Dec 1979/15:00 hrs/MT; FQ Bohadschia similis Several ind. Actinopyga miliaris Several ind. Babin (personal Ué Bay 26 Nov 1979/night/LT; LQ communication) Bohadschia argus 3 ind. Menou (personal Coco Islet 5 Dec 1979/night/MT; NM communication) Strichopus variegatus Laboute (personal Croissant Islet 20 Feb 1980/day/4 d after NM communication) Holothuria scabra versicolor Laboute (personal Croissant Islet 25 Feb l980/2 d after FQ communication)

Table 5. Parameters at first sexual maturityof New Caledonia holothurians. LT,,: length first maturity; WT,,: total weight at first maturity; WD,,: drained weight at first maturity; LT, and WD,: maximum length and maximum drained weight

Habitat LT50 LT/LT, WT50 WD,, WD.50/WDM Species (") (%I (g) (g) (%I Slopes and passes Holothuria nobilis 260 46 800 580 24 Holothuria fuscogilva 320 56 1 175 900 35 Holothuria fLìscopunctata 350 46 1 220 870 27 Thelenota ananas 300 45 1230 1150 20 Outer reef flats Actinopyga mauritiana 220 55 3 70 250 31 Actinopyga echinites 120 32 90 75 12 Inner lagoon and reef flats Holothnria scabra 160 41 185 140 13 Holuthuria scabra versicolor 220 46 490 320 17 St ich opus variegatus 210 47 560 450 22 Holothuria aira 165 51 160 110 32 C. Conand: Reproduction of New Caledonian holothurians ' -. Q 10' CI3 - - Am b 80 A 400 - I- I- I I I? b II AO $ ' 60 A 300 -I s 4 Fig. 6. Relative fecundities, per ovary > b >. O 40 200 2 and body wall weight unit, in relation to Hn > m Hs O the mean body wall weight of the spe- CI b A cies. Ae: Actinopyga echinim; Am: A. . b c) UI b . u1 mauritiana; H fg: Holothuria.fuscogilva; c" 20 b 100 > Hsv sv XfQ Hfp: H. fuscopunctata; Hn: H. nabilis; b > O A o Hs: H. scabra; Hsv: H. scabra versicolor; A b Ta O H!pA O Sv: Sticliopus variegatus; Ta: Tlielenota D A O ananas I , I I I l I I 400 800 1200 1600 BODY WALL WEIGHT ( G )

Table 6. Absolute and relative fecundities per ovary and per eviscerated weights (g) of New Caledonia holothurians. m: mean value; s: standard deviation

Habitat 11 Absolute fecundity Relative fecundity/ Relative fecundity/ Species (iob3 oocytes) g ovary weight g eviscerated (lob3 oocytes) weigth oocytes)

Slopes and passes Holotliuria riobilis 24 Minimum 13 281 m 208 m 28 Maximum I8 517 S 38 S 14

Holothuria fuscogilva 5 Minimum 6 387 m ' 128 m 7 Maximum 14 210 si,22 S 2 Holothuria fuscopunctata 11 Minimum 295 m 44 m 4 Maximum 13 112 S 15 S 2 Thelenota ananas 5 Min im u m 2 239 m 14 m 2 Maximum 1861 S 10 S 1

Outer reef flats Actinopyga mauritiana 5 Mimimum 23 683 m 389 m 80 Maximum 33 790 S 51 S 13 Actinopyga ecliinites 25 Minimum 3 831 m 333 m 59 Maximum 25 O44 S 64 S 24

Inner lagoon and reef flats Holothuria scabra 5 Minimum 9 207 m 133 m 31 Maximum 11313 S 18 S 9 Holothuria scabra versicolor 12 Minimum 2 296 m 93 m 11 Maximum 18 108 S 23 S 5 Siicliopus variegatus 5 Minimum 1243 m 120 m 9 Maximum 12 585 S 11 S 2

value. This is the result of sampling individuals of differ- ripe oocytes and high fecundity, while H. fuscopunctata ent sizes and of the variability of the mature gonad has large oocytes and low fecundity. Fecundity related to weight. The interspecific variation ranged from a mini- eviscerated weight (FRG) is also variable between the mum of 295 x lo3 oocytes in H. fuscopunctata to a maxi- species. mum of 33 790 x lo3 oocytes in Actinopyga mauritiana. Relative fecundity values FRO and FRG are correlated with the mean body wall weight of the species (Fig. 6). Fecundity related to ovary weight (FRO) varied inter- Discussion specifically with oocyte size, the importance of the most advanced mode of oocytes, and the amount of somatic The present study described the reproductive cycles, mea- tissues in the gonad. The small saccules of the gonads in sured fecundity and reproductive output of nine species the Stichopodidae have more epithelial tissue and the from the lagoon of New Caledonia. Since Bakus (1973) fecundity is low. The species of Actinopyga have small review which pointed out the rarity of reproductive stud- C. Conand: Reproduction of New Caledonian holothurians 447

¡es of tropical holothurians, a number of publications Body size is an important parameter for interpreting have concerned Indo-Pacific tropical aspidochirotids the variations in reproductive output and index, both from the Holothuridae family: Holozhuria leucospilota by in terspecifically and intraspecifically. Interspecific differ- Franklin (1980), H. atra, H. edulis, H. impatiens, H. ences must be examined separately for males and females scabra by Harriot (1980,1985). This species has also been on account of the dimorphism. For most of the species studied by Shelley (1981), Ong Che and Gomez (1985) (with the exception of Holothuria fuscogilva where the and Conand (1986). Conand also described the reproduc- sample size was small and the standard error high), the tive biology of H. nobilis, H. fuscogilva (1981, 1986), and reproductive output increases with the body size. An in- of Actinopyga echinites (1982, 1986). In the Stichopodi- verse relationship is shown by the reproductive index, dae family Stichopus ckloronotus has been studied by smaller species having higher values, with the exception Franklin (1980), Thelenota ananas and S. variegatus by of H. atra. In this species asexual reproduction by fission Conand (1 981, 1993). These studies described the phases may complicate the interpretation (Ebert 1978, 1983, Co- of the reproductive cycles. nand and De Ridder 1990). The energetic costs of fission and subsequent regeneration may decrease the sexual re- production capacity. Although the data published on Gonad anatomy, maturity stages other species are not directly comparable, as different weights and indices have been used, the same trend ap- All the species studied here are dioecious and itero- pears in the reproductive index of H. atra, H. impatiens parous. Differences observed in the morphology of the and H. edulis, studied by Harriot (1985) and in A. fecund tubules in the gonads amongst the Stichopodidae echinites and H. scabra studied by Shelley (1981). has led to the distinction of several groups. The first one Intraspecific differences are not easy to determine for comprises some temperate species and is based on de- several reasons: the high variance observed in gonad scriptions by Mitsukuri (1903) and Levin (1982) for Sti- weights and gonad indices in most holothurians, the chopus japonicus, Smiley and Cloney (1985), Cameron modality of the onset of the first sexual maturity which is and Fankboner (1986) for S. californicus and Sewell poorly known, the size distribution in the holothurian (1992) for S. mollis. In this group, the tubules are elongat- populations often composed of a large proportion of ma- ed and similar to the Holothuridae. The second group, ture adults. Intraspecific differences in reproductive out- characterised by the presence of fecund saccules is subdi- put and indices therefore necessitate more comparative vided into species with branched tubules as Thelenota studies using large Bãmples and standardized weight ananas, S. chloronotus as observed by Franklin (1980), parameters, such as body wall (or eviscerated weight) and Conand (personal observation) and 1: anax (personal ob- gonad weight, both in wet, dry and ash-free dry weight servation) but not observed by Lamberson (1978). Only units. one species, S. variegatus, has unbranched tubules with The size of the eggs is an important parameter of the saccules (Conand 1993). One implication of the presence reproductive strategies. Its implications in functional and of saccules is a probable increase of the peritoneum and adaptative aspects has been discussed in detail for echi- connective tissue compartments compared to the noids and asteroids by Emlet et al. (1987). In the aspi- gametes. Experimental studies are needed following Smi- dochirote species studied the modal size of the mature ley's model (1988) on the resorption of spent tubules and oocytes varies only between 150 and 210 pm. This is an the role of the nutrients derived from phagocytosis to indication of a probable planktotrophic development if determine if this organisation has functional conse- compared with the planktotrophic echinoids and as- quences. teroids. No correlation is found with the size of the spe- Within the nine species, the size frequency distribu- cies or with the family. The same statement holds with the tions of the males and females are similar (Conand other data on oocyte diameters for Holothuria edulis: 1989a), but ripe females have larger gonads in stage IV 103 pm; H. impatiens: 184 pm; H. atra: 88 pm (Harriot which is indicative of the reproductive output and the 1985); H. scabra: 155 pm; A. echinites: 149 pm. The lower mean values of the gonad index, indicative of the repro- values found by these authors result from the method ductive index (Lawrence 1987). The gonadal tubules are used: Bouin fixation shrinks eggs. H. parvula (formalin also shorter and wider in females. As the gonad structure fixation) oocytes measure only 93 pm (Emson and is comparable in both sexes, the difference indicates a Mladenov 1987). This species and H. atra are fissiparous smaller reproductive output in males. This dimorphism and have relatively small eggs. shown by Holothuridae and Stichopodidae from the New Caledonian lagoon has also been observed in other aspidochirotes: Stichopus japonicus (Choe 1963), Holo- Reproductive cycles, spawning behaviour thuria floridana and H. mexicana (Engstrom 1980), H. atra, H. impatiens, H. edulis, H. scabra (Harriot 1980), All the species studied in New Caledonia show an annual H. scabra, Actinopyga echinites (Shelley 1981), Parasti- reproductive cycle. Three main patterns in reproductive clzopus californicus (Cameron and Fankboner 1986), S. seasonality were observed. mollis (Sewell and Bergquist 1990), and H.forskali (Tuwo (1) Most species spawn during the warm water season and Conand 1992). This could mean that either females (December to February in New Caledonia). This agrees eat more, or use the absorbed material more efficiently, with observations of other tropia1 species: Holothitria leu- or use it preferentially for the gonads. cospilota (Franklin 1980); H. impatiens (Harriot 1980); ’ 448 C. Conand: Reproduction of New Caledonian holothurians Actirzopyga echirlites (Shelley 1981). For the last species Pearse et al. (1988) observed simultaneous spawning of the reproductive phases are more precisely defined in six species of echinoderms, and McEuen (1 988) presented New Caledonia (Conand 1982) than in Papua New a review of the published observations for all holothurian Guinea. This agrees with Pearse’s observations (1968) of orders. The observations made in New Caledonia con- more restricted spawning seasons at higher latitudes. Sev- firm the spawning behavior of aspidochirotids first de- eral examples for echinoids are given in Giese and Kana- scribed from Bohadsclria nzarntorata in aquarium by tani (1987). The temperate species Stichopus japonicus Mortensen (1937). The raised genital papilla probably (Tanaka 1958), Parastichopus califorriicus (Cameron and helps dissemination of eggs and sperm. The observations Fankboner 1986), and S. mollis (Sewell and Bergquist presented here are the first report of field spawning for 1990, Sewell 1992) also spawn during summer. Actinopyga nriliaris, Bohadschìa similis, B. argus, (2) Holothuria scabra has a biannual cycle in India Holotliwia,JZavoniaculata, H.scabra versicolor. On sever- (Krishnaswamy and Krishnan 1967), (Harriot al instances, H. nobilis collected for monthly sampling 1980), Papua New Guinea (Shelley 1981) and in the spawned in the tanks on the way to the laboratory. Three (Ong Che and Gomez 1985). In New Caledo- factors could be involved in the tanks: the increase in nia, as in the other localites, the warm season spawning water temperature, crowding and agitation. Other obser- is dominant and the secondary peak is smaller and more vations from the Great Barrier Reef can also be added. variable. This pattern has also been found for Stichopus Silver (personal communication) observed B. graeffei cltloroizotus (Franklin 1980) and H. atra in Australia spawning at Lizard Island during an afternoon low tide (Harriot 1980, Conand and De Ridder 1990). in January, and Franklin (1980) observed a loose correla- (3) One species, Holothuria nobilis shows a cycle tion with full and new moon for H. leucospilota spawning marked by a long spawning period during the cool season simultaneously in separate aquaria in December 1977 and the beginning of the warm season. and January 1978. Simultaneous spawning has therefore In New Caledonia none of the species studied spawns been. observed for conspecifics of the Holothuridae. This continuously, or without seasonality, as does Holothuria synchronization might be a response to a pheromone. No edulis (Harriot 1985) and many deep-sea species (Tyler et “pseudocopulation” as mentioned by McEuen (1 988) has al. 1985). Most species have, nevertheless, a few mature been observed for New Caledonia holothurians. Envi- individuals in most samples except during the resting ronmental conditions during the spawning events could phase. They cause the high variability of the gonad help determine the triggering stimulus: the observations weights and indices. were made primarily during the afternoon and the night, In holothurians, as in other marine invertebrates, the so light changes could be evoked. No clear relation ap- circannual reproductive cycles probably result from in- pears with the tidal or the lunar cycles. teractions between endogenous rhythms and exogenous environmental timers (Giese and Kanatani 1987). The variety described in these holothurians from New Cale- First sexual maturity and fecundity donia argues in favour of the existence of specific innate rythms. Environmental cues could then allow in- In these populations of iteroparous species, first sexual traspecific temporal synchronization. For most species, maturity is attained progressively by the individuals be- the growing and maturing phases occur during the warm- tween a size where they are all immature and a size where ing period when the days become longer. This results in all are maturing. Size at first maturity is related to the spawning during the warm season. The planktotrophic mean size of the species; it is attained earlier in the small larvae can therefore take advantage of the rich phyto- species Actinopyga ecliinites, A. mauritiana and Holot- . Thus at the Noumea coastal station (see Fig. l) huria scabra. In other studies only approximative mean the chlorophyl a content (Dandonneau personal commu- size for maturity has been given. Yet this parameter is nication) was relatively stable, between 0.1 and 0.3 mg important for understanding the change in allocation of mb3, between July 1986 and February 1987, and more energy from somatic growth to reproduction. The study variable with higher concentrations, up to 0.7 mg m-3, of their fecundity has shown a few characteristics of these between March and June. The inverse timing described species. Gross differences appear between families. Sti- for Holothuria nobilis is more questionable. Does it result chopidae are less fecund, a fact which can be related to from different critical values of the environmental their gonad anatomy. Absolute fecundities are rather parameters, or is it an adaptation to the competition with variable amongst Holothuridae. Interspecies compari- other species, particularly with H.fuscogilva with which sons of relative fecundity show that the small species are it has often been confused? Similar arguments can be more fecund. Within a species, fecundity increases with evoked to explain the semiannual cycle of H. scabra and body size. its difference with the variety (or sibling species?) H. scabra versicolor. Some authors (Krishaswamy and Krishnan 1967, Ong Che and Gomez 1985) considered Life history strategies salinity as the environmental cue for H. scabra. No com- parable semiannual changes in salinity occur in New The aspidochirotes are usually considered to share the Caledonia and Australia (Harriot 1982). same strategy. As a whole, they display the same deposit- Observations of spawning in the field are few for the feeding and locomotion habits, iteroparity and high Indo-Pacific aspidochirotids (Giese and Kanatani 1987). longevity, as pointed out by Lawrence (1990). They also C. Cpand: Reproduction of New Caledonian holothurians 449 Table 7. Demographic features of some New Caledonia holothurian populations arranged by increasing mean size of species. *: low value; **: medium value; ***: high value Habitat Length First Relative Oocyte Population density Specks (or weight) maturity fecundity diameter Numbers Weights

Outer reefs flats and passes * * * ** ** Actinopyga echinites * * *** * *** *** Acrinopyga inauriliana * ** *** * *** *** Inner lagoon and reef flats Holorhuria scabra ** * ** ** *** *** Holothuria scabra versicolor ** * ** *** ** ** Stichopus variegatus ** ** * ** ** ** Slopes and passes Holothuria fuscopunctata *** *** * *** * ** Holothuria nobilis *** ** ** * * * Holothuria fuscogìlva *** *** * ** * * Thelenota ananas *** ** * *** * **

show relatively large size, stable densities and various Bakus, G. J. (1973). The biology and ecology of tropical holothuri- defenses against predation (toxicity, cuvierian tubules, ans. In: Jones, I. O. A., Endean, R. (eds.) Biology and geology evisceration), which correspond to K-strategies in the of coral reefs, Vol. II. Academic Press, New York, p. 325-367 Birkeland, C. (1989). The influence of echinoderms on oral-reef r-K-selection theory. They yet have high fecundities and communities. In: Jangoux, M., Lawrence, J. M. (eds.) Echino- small eggs, but probably low and sporadic recruitment. derm studies, 3. Balkema, Rotterdam, p. 1-79 The demographic characteristics of the different species Cameron, J. L., Fankboner, P. V. (1986). Reproduction biology of studied in New Caledonia are presented synthetically in the commercial Parastichopus californicus (Stimp- Table 7, arranged by increasing mean size of the species. son) (Echinodermata, Holothuroidea). I - Reproductive period- Interspecific comparisons clearly show a gradient related icity and spawning behavior. Can. J. Zool. 64 168-175 Choe, S. (1963). Biology of the Japanese Common Sea Cucumber to the mean size of the species. Smaller species, such as Stichopus japonicus, Selenka. Pusan National University, Pusan Actinopyga echinites and A. mauritiana are situated to- (in Japanese) ward the r, whereas larger species, such as Holothuria Conand, C. (1981). Sexual cycle of three commercially important nobilis and Thelenota ananas are toward the K of a r-K- holothurian species (Echinodermata) from the lagoon of New continuum. The former live in outer reef flats which are Caledonia. Bull. mar. Sci. 31: 523-544 high energy habitats with higher productivity and shorter Conand, C. (1982). Reproductive cycle and biometric relations in a population of Actinopyga echinites (Echinodermata: Holo- duration than lagoon floors or deeper coral slopes. thuroidea) from the lagoon of New Caledonia, Western Tropical Growth and morality values for is ananas and Stichopus Pacific. In: Lawrence, J. M. (ed.) Echinoderms: proceeding of chloronotus (Conand 1989 b) show that the former has a the intemational conference Tampa Bay. Balkema, Rotterdam, slower growth and higher longevity compared to the lat- p. 437-442 ter. Conand, C. (1986). Les ressources halieutiques des pays insulaires This comparative approach, at the population level, du Pacifique. Deuxième partie: les Holothuries. F.A.O. Doc. Tech. Pêches, 272.2, F.A.O., Roma has shown that there is a gradient in the strategies Conand, C. (1989a). Les holothuries aspidochirotes du lagon de amongst coral-reef aspidochirotes. A better basic under- Nouvelle-Calédonie: biologie, écologie et exploitation. Etudes et standing of their acquisition of energy and growth, as thèses, ORSTOM, Paris well as of the productivity of the various habitats is yet Conand, C. (1989 b). Comparison between estimations of growth required for a more complete interpretation. and mortality of two Stichopodid holothurians: Thelenota ananas and Stichopus chloronotus (Echinodermata: Holo- Acknowledgenzents. I thank O.R.S.T.O.M. (Institut Français de thuroidea). In: Proc. 6th int. coral Reef Symp. (1989) 2 661 -665 Recherche Scientifique pour le Développement en Coopération) [Choat, J. H. et al. (eds.) Sixth Intemational Coral Reef Sympo- which supported this work and G. Bargibant, C. Hoffschir, P. sium Executive Committee, Townsville] Laboute, J. L. Menou and P. Tirard for field and laboratory assis- Conand, C. (1993). Ecology and reproductive biology of Stichopus tance. I am grateful to J. M. Lawrence and M. Glemarec for helpful variegatus and Indo-Pacific coral reef sea cucumber (Echinoder- discussions and comments. Contribution # 93001 from URA mata: Holothuroidea). Bull. mar. Sci. 52 (in press) CNRS 1513. Conand, C., Chardy, P. (1985). Les holothuries aspidochirotes du lagon de Nouvelle-Calédonie sontelles de bons indicateurs des structures récifales? In: Proc. 5th int. coral Reef Congr. 2: 291 - 296 [Gabrié, C. et al. (eds.) Antenne Museum-EPHE, Moorea, French Polynesia] Literature cited Conand, C., De Ridder, C. (1990). Reproduction asexuée par scis- sion chez HoIothuria awn (Holothuroidea) dans des populations Bagenal, T. B. (1973). Fish fecundity and its relation with stock and de platiers récifaux. In: De Ridder, C., Dubois, P., Lahaye, M. recruitment. Rapp. P.-v Réun. Cons. int. Explor. Mer 164: 186- C., Jangoux, M. (eds.) research. Balkema, Rotter- 198 dam, p. 71-76 .c 450 C. Conand: Reproduction of New Caledonian holothurians

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